Monday, October 31, 2016

Recently, Sarah Kopac and Jonathan Klassen described a new
model to understand the evolution of host-microbe symbioses in their paper “Can They Make It on Their Own? Hosts, Microbes, and the Holobiont Niche”.
In this model, hosts and microbes can change the shape of their respective
niches, and thereby the context in which selection can act. This permits a test of holobiont theory by identifying instances where an organism’s
phenotype depends on its symbiotic partners. Jonathan answered the following
questions, incorporating feedback from Sarah. Be sure to read all the way through.

1.What motivated the theory reported in
the paper?

It feels a bit murky now, but looking
back I think there were three main motivations. First, we were quite struck by
how host-microbe relationships can be thought of as a community ecology
problem, i.e., where and how do interspecific relationships form and what is
their outcome? So because much of the holobiont/hologenome literature has
started from a population-genetics perspective (e.g., http://journal.frontiersin.org/article/10.3389/fmicb.2014.00046/full),
we thought that drawing from a different intellectual tradition might be a way
to get beyond current sticking points in the field's discussion. Another interesting aspect of the community ecology
perspective is that it defines the context in which selection might act, leaving whether or not
selection does act as a separate
question. I think that it is too common to assume selection without rigorously
testing against alternative hypotheses, e.g., drift or dispersal limitation, to
our detriment. Second, we wanted to strongly highlight how any selection that
did occur likely impacted hosts and microbes differently, e.g., because
microbes have shorter lifespans and higher population sizes and dispersal rates
than their hosts (http://doi.wiley.com/10.1002/bies.201500074).
Third, one major take-away from my years of reading the lovely Dynamic Ecology
blog (https://dynamicecology.wordpress.com/)
is that mathematical models have a rigor and testability that verbal models
cannot match, and thereby overcome the potential for verbal models to become
misconstrued. Expressing our ideas mathematically so that they would be
unambiguously testable therefore became an important goal.

2.How did you come up with the title?

Truthfully, this was a revision suggested by one of the
reviewers. (And they were right - thanks!) Sarah came up with this version, and
I think it’s great because it really captures the key question of our model: do
host-microbe interactions matter for the evolution of either partner? I think
the answer is that it depends on the context, i.e., does the interaction change
the shape of either partner’s niche in a way that changes how selection might
act? I also love how (in my mind at least) there’s a U2 reference - https://www.youtube.com/watch?v=CuDqHtAR6L8.
I’ve long been a fan.

3.When and how did you two come together and
agree on this paper? Were there varied opinions about how to approach the
problem?

We agreed on the central idea of explaining holobionts in
terms of niche theory early on, and so were unified on that front. There was a
bit of divide and conquer after that, with Sarah focusing more on the examples
of different niche shifts and I focusing more on the models themselves. Then we came back together and made sure that
the examples we saw in the literature could be explained using our models.
I found it very helpful to get someone else’s view of the literature –
accurately synthesizing everything that’s out there alone would have been a
massive challenge.

4.What are the
most salient findings?

I think that it is striking how our models are agnostic
towards any particular mechanism of host-microbe interaction. For example, a
similar shift in a host’s niche could be result from that host selecting
microbes with a particular trait from the environment each generation, or it
could be due to tight host-microbe co-evolution and vertical transmission. The
important thing is that in either case the interaction changes the shape of a
host’s niche in a way that selection might act upon. Both partners are
therefore needed to completely describe host evolution. I am also struck by how
our models accommodate the full diversity of symbiotic relationships, including
the various forms of conflict that change the shape of a host’s niche but in a
different way than mutualism. Finally, it seems that the symbiosis community
has already been at least implicitly thinking in terms of our model because it
was easy to find studies that had already tested it by changing one parameter
at a time, e.g., by swapping microbiomes between constant host genotypes and
vice versa. Hopefully our work can guide future experiments that continue to
explicitly test these ideas.

5.What are the
most crucial questions moving forward in your mind? What do you want
to do next?

Perhaps one problem with our model is that precisely
defining the shape of an organism’s niche is fiendishly difficult, mostly
because there are a potentially infinite number of niche axes to consider. I
think it will be interesting to understand how many of these are actually
needed to come up with an accurate niche description. For example, to what
extent to do microbe-microbe interactions need to be considered to describe how
microbes alter a host’s niche? I also think it will be critical to learn more
about microbes in non-host environments so that we can determine if hosts
modify the niches of their microbial symbionts outside of obvious cases like
intracellular mutualists and pathogens. Lastly and as described above, I think
it will be crucial to explicitly test whether any host-microbe interaction
phenotype actually arises due to selection, e.g., vs drift or dispersal
limitation.

6.Anything else
you want to add?

Thanks to our colleagues in the symbiosis field for being so
collegial, even in disagreement! I look forward to increasing the rigor of our
studies, and to a deeper understanding of how ecology and evolution both shape
host-microbe relationships.

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Biography

Dr. Seth R. Bordenstein is
an Associate Professor of Biological Sciences and Pathology, Microbiology, and Immunology at Vanderbilt University, Nashville, TN, lab home page. He received his B.S., M.S. and Ph.D. from the University of Rochester and held a Postdoctoral Fellowship from the National Research Council at the Marine Biological Laboratory in Woods Hole, MA. His laboratory studies evolutionary biology, microbiology, and virology, and he is most well known for his work on the microbiome, symbiosis, speciation and antibiotic discovery. Dr. Bordenstein is the founding director of the worldwide, project-based, HHMI science program called Discover the Microbes Within! The Wolbachia Project (main website & facebook page). His research and science education activities have been highlighted in various popular science media including a documentary on bacterial symbiosis, the New York Times, National Geographic, Discover Magazine, PBS, Scientific American, BBC Radio, among others. Twitter: @Symbionticism.